L
Journal of Experimental Marine Biology and Ecology 243 (2000) 261–282
www.elsevier.nl / locate / jembe
Predation and sediment disturbance effects of the intertidal
polychaete Nereis virens (Sars) on associated meiofaunal
assemblages
a ,* a b a
G. Tita , G. Desrosiers , M. Vincx , C. Nozais
a
´ ´ ` ´
Universite du Quebec a Rimouski, Institut des Sciences de la Mer (ISMER), 310 allee des Ursulines, ´
Rimouski, Quebec, G5L 3A1 Canada
b
University of Gent, Biology Department, Marine Biology Section, Ledeganckstraat 35, B-9000 Gent, Belgium
Received 5 February 1999; received in revised form 4 August 1999; accepted 5 August 1999
Abstract
A microcosm experiment was carried out to determine the effects of the activity of the burrowing polychaete Nereis virens (Sars) on the associated meiofauna. The sediment basin (76341 cm) was filled with 10 cm of sandy sediment previously sieved with a 1-mm mesh to remove any undesired macrofauna and macrodetritus. Fifteen 13-cm long polyvinyl-chloride (PVC) tubes (I.D.510 cm) were pushed into the sediment to partition treatments. Nereis were added to the tubes at two densities, low (N51) and high (N53). Five tubes were used as controls (no Nereis), while two sets of five tubes were used for the low (L) and high (H) density treatments, respectively. After 14 days, meiofauna was sampled by coring. Cores were cut into three slices: surface (0–1 cm), subsurface (1–5 cm), and deep (5–10). High densities of Nereis (H) significantly affected nematodes, harpacticoid copepods, and nauplii abundance. However, lower abundances were found only in the top cm of the sediment. Moreover, a significant number of dead nematodes found in this sediment layer of treatment H allowed a distinction between sediment disturbance effects and predation effects. Sediment disturbance caused by Nereis may be related to an intensive ‘‘ploughing’’ of surface sediment during food-searching activity. Diversity indices were affected only in the top cm of the sediment with generally lower values in treatment H. Differences in the relative survival of the different feeding groups were found in treatment H, where microvores and deposit feeders respectively showed greater and lower survival. Multivariate analysis (multidimensional scaling) revealed significant differences in nematode species com-position among treatments in all sediment layers. It is concluded that N. virens significantly affects meiofauna mostly by disturbance of the top cm of the sediment where its predation represents an influent force as well. The structure of nematode assemblages in subsurface and deeper sediment
*Corresponding author. Fax 11-418-724-1842. E-mail address: gugliemo [email protected] (G. Tita)]
layers is also affected, most likely by changes in redox conditions caused by the bioirrigating effects of Nereis burrows. 2000 Elsevier Science B.V. All rights reserved.
Keywords: Nereis; Disturbance; Predation; Community structure; Meiobenthos; Nematodes; Microcosm experiment
1. Introduction
Several studies have shown the importance of infaunal polychaetes in structuring macrofaunal benthic assemblages either by trophic interactions (i.e. competition and predation) or by sediment disturbance (Fauchald and Jumars, 1979; Witte and de Wilde, 1979; Brenchley, 1981; Wilson, 1981; Commito and Shrader, 1985; Ronn et al., 1988). Commito (1982) and Ambrose (1984a,b,c) showed that nereid polychaetes play a significant role in regulating the densities of infaunal amphipods, bivalves, and annelids. Other studies suggest that nereids may be an important structuring agent of meiofaunal assemblages as well, again through predation or sediment disturbance.
¨
Goerke (1971) defined the polychaete Nereis diversicolor (Muller) as an opportunistic omnivore including meiofauna in its diet, and Reise (1979) demonstrated that N.
diversicolor can have a significant negative impact on meiofaunal abundance. Ronn et
al. (1988) stated that this polychaete ‘‘must be considered as an important structuring force in brackish-water soft-bottom habitats, either by direct predation or by dis-turbance’’. Olivier et al. (1993) showed through gut content analysis of Nereis virens (Sars) that adults of this species are almost exclusively carnivores feeding on small macrofauna and meiofauna, whereas juveniles are deposit-feeders. A comparative study between N. diversicolor and N. virens showed that these two burrowing species have very similar feeding strategies (Olivier, 1994). Both of them use two different food-searching strategies (Goerke, 1971, 1976; Miron et al., 1992a,b; Olivier, 1994). The first strategy (surface searching) consists of extending a third of their body length from their burrow to search for detritus particles or small macrofaunal prey. The latter are attacked with a rapid bound and seized with the eversible pharynx and large jaws typical of
Nereis. Using this same tactic, Nereis can ‘‘sweep and plough’’ the surface of the
greater meiofaunal abundance in deeper sediment layers near macrofaunal burrows suggesting a promotive effect of these biogenic structures.
In spite of the above mentioned studies, indicating that Nereis have an influence on meiofauna, Kennedy (1993) concluded after a 6-day field experiment that meiofauna were unaffected by the presence of N. diversicolor.
N. virens is one of the dominant macrofaunal species of the soft-bottom intertidal zone of the St. Lawrence Estuary (Canada) (Desrosiers et al., 1980, Desrosiers and
ˆ
Brethes, 1984), and represents one of the most influential biological components of the local intertidal ecosystem (Caron, 1995).
The aim of the present study was to determine if Nereis is an effective determinant of meiofaunal densities and nematode assemblages structure. If it is, two questions must be addressed: (1) Is the effect of Nereis limited to the surface layer of the sediment, where it feeds, or does it affect deeper layers as well? (2) Do different densities of Nereis result in different degrees of structuring effect on nematode assemblages? In order to answer to these questions, a microcosm experiment was carried out to observe the effects of N.
virens on the meiofauna.
2. Materials and methods
2.1. Experimental design
`
A 14-day microcosm experiment was conducted at the Pointe-aux-Peres nearshore
´ ´ `
station of the Universite du Quebec a Rimouski (UQAR) on the south shore of the St. Lawrence Estuary (Canada). On September 10, 1997, the top 10 cm sediment was collected from the mid tidal zone of a sheltered inlet located in the Parc provincial du
`
Bic, 45 km west of Pointe-aux-Peres. The sediment was sieved through a 1 mm mesh in order to eliminate the bulk of macrofauna and macrodetritus, and distributed evenly in a 10 cm layer in a poly(vinyl chloride) (PVC) basin (76 L341 W335 H cm) after being thoroughly mixed to ensure homogeneity. A sample of the sieved sediment was used for granulometric analysis (median590mm; silt-clay514%) and organic matter (1.4% of sediment dry weight; combustion at 5008C for 6 h). Fifteen PVC tubes (internal diameter510 cm; length513 cm) were inserted into the sediment (Fig. 1). Tubes protruded 3 cm out of the sediment and had four holes (diameter55 mm) drilled on opposing walls just above the sediment–water interface to allow water circulation. The holes were covered with a 500-mm mesh gauze in order to prevent Nereis individuals from leaving their respective tube. The basin was placed in a room with constant temperature (138C) and a 12:12 h L:D photoperiod. The temperature corresponded to the mean summer water temperature in the field, and the photoperiod was an approximation of the natural summer photoperiod. Sea water in the basin had a 10 cm depth above the sediment and was changed every 48 h with water collected directly from the sea by a pumping system of the station and previously brought to the experimental temperature. Water aeration was maintained with six air stones. In order to allow surface sediment to remain undisturbed, water change was made as slow as possible (water level increase /
21
Fig. 1. Experimental design: position of treatments (randomly selected) in the basin; C5controls (no Nereis); L5low density of Nereis (N51); H5high density of Nereis (N53). Internal diameter of treatment tubes510 cm. Aeration was insured by six air stones (a) evenly spaced along the side of the basin.
Individuals of Nereis were collected on September 11, 1997, from the same station as the sediment sampling. At this site, Nereis individuals have a mean body size intermediate between mature adults, which primarily inhabit the lower tidal zone, and juveniles, which inhabit the upper tidal zone (Caron et al., 1995). Individuals were
21
selected according to body length (7.361.0 cm ind. ) and body wet weight (6846151
21
mg ind. ). Two h after collection, the polychaetes were placed in a basin containing aerated marine water located in the same temperature-controlled room. Twenty-four h after polychaete sampling, Nereis individuals were added to the cores of the sediment basin according to the following design: (i) five control cores (C) with no Nereis; (ii) five low-density cores (L) with one individual of Nereis; (iii) five high-density cores (H) with three individuals of Nereis. Low and high densities of Nereis corresponded to approximately two- and five-times the normal mean density in the field (75625 ind.
22
m , Caron et al., 1995). This was selected following the principle that, at greater experimental densities over a short period of time, the predator should induce a similar effect to normal densities over a longer time (Raffaelli et al., 1989). It is worth noting,
2
however, that densities reported by Caron et al. (1995) are integrated on 1 m , and that, at smaller spatial-scales, according to its patchy distribution this polychaete may show densities comparable to those used in our experiment (A. Caron, personal communica-tion). In order to avoid any escape of Nereis individuals, 2-mm mesh grids were fixed to the top of each core including the control cores.
2.2. Sampling
was collected (i.e. five replicates per treatment). Core samples were sectioned from the top into three slices, surface (0–1 cm), subsurface (1–5 cm), and deep (5–10 cm), and fixed with 4% formalin. Meiofauna extraction was done by centrifugation with Ludox TM (Heip et al., 1985) after washing samples over a 63-mm mesh sieve. Meiofauna were then counted under a dissecting microscope. Ninety nematodes per core slice were randomly selected and mounted on slides in anhydrous glycerol for identification at genus level, or species when practicable, using higher resolution microscopy. In samples of the 0–1 sediment layer of treatment H, 90% of individuals were found to be dead at the sampling time (see Results). The whole nematodes (dead1live) of these samples were therefore mounted on slides in order to have an acceptable number of live individuals for statistical analyses. Genus and species identification was based on Platt and Warwick (1983, 1988), and Hopper (1969). Assemblage analysis was restricted to the nematode meiofaunal component only. All individuals of Nereis were recovered alive and in good condition at the end of sampling procedure.
2.3. Data analysis
Abundances of the two main meiofaunal groups (nematodes and harpacticoid copepods) were used as a primary indicator of Nereis influence. Juvenile copepods (nauplii) were counted separately from adults (mentioned as copepods herein) and considered as a third meiofaunal group. Abundance data were ln-transformed for comparison among treatments in order to achieve the analysis of variance (ANOVA) assumptions (normality: Kolmogorov–Smirnov test; equal variance: Levene Median test). Effects on nematode species diversity was studied using four indices: (1) the number of species, N; (2) the Margalef’s species-richness-weighted diversity index, SR (Margalef, 1958); (3) the Shannon index (calculated with Log ), H2 9 (Margalef, 1958); (4) the evenness, J9 (Pielou, 1966). Statistical differences between diversities of treatments were studied with untransformed data because ANOVA assumptions were achieved. The Student–Newman–Keuls (SNK) procedure was used for all pairwise multiple comparison between treatments.
The effects of Nereis on the different components of nematode assemblages were determined using a multidimensional scaling ordination (MDS) with different degrees of data transformation. Untransformed data analysis is more sensitive to changes in abundance of the dominant species, while increasingly severe data transformations (œ andœœ) are more sensitive to changes of abundance of intermediate and rarest species (Clarke and Warwick, 1994). The MDS analyses were run on Pearson correlation matrices using the SYSTAT.7 software package (Wilkinson, 1997). One way ANOSIM (analysis of similarities) was carried out to determine differences between nematode assemblages in different treatments and sediment depths. SIMPER (similarity per-centages) was used to determine the contribution of individual species towards dissimilarity between treatments. ANOSIM and SIMPER were run using the PRIMER (Plymouth Routines in Multivariate Ecological Research) (M. Austen, Plymouth Marine Laboratory, personal communication).
3. Results
3.1. Influence on abundance of meiofauna
More than 98% of total meiofauna, in all treatments, were represented by nematodes (|80%), copepods (|7%), and nauplii (|12%). However, in the 0–1 cm layer of treatment H, almost 90% of the nematodes that were counted under the dissecting microscope were found to be dead at the time of sampling when observed at higher resolution microscopy (Fig. 2). Dead individuals were identified by a relatively advanced decomposition of internal anatomy indicating that death probably occurred several days before sampling. This massive mortality was interpreted as a consequence of Nereis sediment disturbance. In the 0–1 cm layer of treatment H, ‘‘live-nematode’’
abundance (2868 individuals) was significantly lower than ‘‘dead-nematode’’ abun-dance (278623 individuals) (t-test, p,0.0001). In the 0–1 cm layer, abundance of ‘‘live’’ nematodes, total nematodes (live1dead), copepods, and nauplii was sig-nificantly lower in treatment H than in controls and treatment L (Fig. 2 and Table 1). Total nematode abundance (dead1live) in treatment H was 39% lower than in the controls. This reduced abundance was interpreted as a gross estimation of Nereis predation effect. The resulting estimation of the ratio dead nematodes / consumed nematodes was 6:4. Abundance of copepods and nauplii in treatment H showed a reduction of the same order with 38 and 48% less individuals, respectively, than in the controls. For these two groups it was not possible to distinguish dead from live individuals as they were not studied at higher resolution microscopy.
No significant difference was found for nematode abundances between treatments in the subsurface (1–5 cm: F53.31, p50.071) and the deep (5–10 cm: F52.10,
p50.166) sediment layers. In these two sediment layers, copepods and nauplii had densities too low to allow statistical comparisons between treatments.
The abundances of live nematodes and total nematodes in the whole sediment cores (0–10 cm) was significantly greater in treatment L than in the controls and treatment H (Fig. 2, Table 1). The greater abundance of nematodes in the whole cores of treatment L compared to controls was due to a greater abundance in the 1–5 and 5–10 cm sediment layers, though not statistically significant when considered in individual layers.
Dead nematodes in treatment H were not considered for assemblage analysis (diversity indices, MDS, and feeding structure), though species were still identifiable.
3.2. Influence on nematode assemblages structure
3.2.1. Univariate analysis
Univariate measures (diversity indices) did not show any significant differences between treatments when considering the whole cores, except for abundance (Figs. 2 and
Table 1
ANOVA results indicating statistic value (F ) and significance level ( p) of tests for differences in abundance (ln-transformation) for the surface sediment layer and the whole cores; SNK test identifies differences among treatments (continuous lines indicate no significant difference)
One-way ANOVA Student–Newmann–Keuls test ( p,0.05)
0–1 cm C L H
‘‘Live’’ nematodes F549.6; p,0.001 —————
Total nematodes (live1dead) F55.3; p,0.05 —————
Copepods F55.2; p,0.05 —————
Nauplii F510.3; p,0.01 —————
Total C H L
‘‘Live’’ nematodes F57.2; p,0.01 —————
3). However, distinct measures of diversity indices for the different sediment layers showed contrasting results. In the 0–1 cm sediment layer, treatment H had significantly lower values for the number of species (N ) and the Shannon index (H9) (Table 2). Inversely, in treatment H, equitability (J9) was significantly greater than in treatment L and tended to be greater, although not statistically significantly, than in controls (Fig. 3 and Table 2).
In the 1–5 cm layer, only the Margalef’s species richness (SR) was found to be significantly greater in treatment H than in C and L (Table 2). No significant difference between treatments was found in the 5–10 cm sediment layer.
Fig. 3. Diversity indices (mean695% CI) for nematode assemblages in specific sediment layers and the whole cores. N5no. of species; SR5Margalef’s species richness; H9 5Shannon’s index (calculated using Log );2
Table 2
ANOVA results indicating statistic value (F ) and significance level ( p) of tests for differences in diversities (no data transformation) for the surface (0–1 cm) and subsurface (1–5 cm) sediment layers; SNK test identifies differences among treatments (continuous line indicate no significant difference)
One-way ANOVA Student–Newmann– Keuls test ( p,0.05)
0–1 cm C L H
N F520.6; p,0.0001 —————
H9 F513.9; p,0.001 —————
J9 F56.1; p,0.05 ————— —
1–5 cm
SR F57.34; p,0.01 —————
3.2.2. Multivariate analysis
The MDS plots with untransformed and œ-transformed data differentiated controls and treatments not only when considering the different sediment layers separately, but also when taking into account the whole cores (Fig. 4). With a more severe data transformation (œœ), samples of all treatments were distributed with no apparent order; for this reason these plots are not reported herein. ANOSIM results show differences between controls and treatments (Table 3). In the 0–1 cm layer, SIMPER results showed that dominant species in controls and treatment L (Eleutherolaimus sp., Anoplostoma
blanchardi, Microlaimus sp. 1, Sabatieria punctata) were the most affected when
associated to high densities of Nereis (Table 4). Species with intermediate abundance (Paracanthonchus caecus, Innocuonema sp., Desmolaimus sp., Theristus (Daptonema)
Table 3
ANOSIM results indicating statistic value (R) and significance level ( p) of tests for differences in nematode assemblage structure between controls (C) and treatments L and H in the different sediment layers and at different levels of data transformation
Data transformation
None œ œœ
R p R p R p
0–1 cm
C L 0.02 0.44 20.03 0.56 0.01 0.44
H 1.00 ** 0.96 ** 0.86 **
L H 0.99 ** 0.96 ** 0.88 **
1–5 cm
C L 0.48 ** 0.33 * 0.16 0.14
H 0.37 * 0.14 0.18 0.03 0.43
L H 0.37 * 0.28 0.56 0.10 0.29
5–10 cm
C L 0.40 * 0.43 * 0.36 *
H 0.42 ** 0.35 * 0.30 *
L H 0.16 0.18 0.27 0.63 0.27 0.71
Total
C L 0.48 ** 0.42 ** 0.19 0.87
H 0.40 * 0.32 ** 0.10 0.21
L H 0.48 ** 0.55 ** 0.46 **
* p,0.05 ( )
** p,0.01 ( )
procerus) were, however, also affected. In the subsurface (1–5 cm) and deep (5–10 cm)
layers, differences between controls and treatments were most evident in the rank of the dominant species, particularly S. punctata, Sabatieria sp. A, and Paramonohystera sp.
3.3. Influence on the vertical distribution of nematode species
Table 4
Results from SIMPER analysis of untransformed data of nematode abundances indicating the contribution (%) of each species to the mean Bray–Curtis dissimilarity term (between parenthesis) for the 0–1 cm (a), the 1–5 cm (b), and 5–10 cm (c) sediment layers; a cut-off of 70% was employed (i.e. when 70% of the total Bray–Curtis dissimilarity term between treatments has been explained by the species which are listed in order of decreasing contribution).
Mean abundance % Cumulative
(ind. / sample) (%)
a)
Treatments compared C L (37.85)
Paracanthonchus caecus 41 13 8.96 8.96 Theristus(D.) procerus 24 39 8.46 17.42 Anoplostoma blanchardi 58 65 8.24 25.66 Innocuonema sp. 27 38 7.88 33.55 Sabatieria punctata 37 43 7.43 40.98 Desmolaimus sp. 27 40 7.19 48.17 Eleutherolaimus sp. 76 69 6.74 54.91 Microlaimus sp. 1 42 41 6.02 60.93 Axonolaimus sp. 18 9 3.86 64.79 Leptolaimus papilliger 12 10 3.63 68.42 Halalaimus sp. 13 12 2.79 71.21
Treatments compared C H (89.41)
Eleutherolaimus sp. 76 3 17.02 17.02 Anoplostoma blanchardi 58 3 12.51 29.53 Microlaimus sp. 1 42 2 9.91 39.45 Paracanthonchus caecus 41 1 9.34 48.79 Sabatieria punctata 37 3 8.06 56.86 Innocuonema sp. 27 0 6.21 63.07 Desmolaimus sp. 27 0.4 5.68 68.75 Theristus(D.) procerus 24 1 5.13 73.87
Treatments compared L H (89.87)
Eleutherolaimus sp. 69 3 15.34 15.34 Anoplostoma blanchardi 65 3 14.74 30.09 Sabatieria punctata 43 3 10.04 40.13 Desmolaimus sp. 40 0.4 9.03 49.16 Microlaimus sp. 1 41 2 8.33 57.49 Innocuonema sp. 38 0 7.79 65.27 Theristus(D.) procerus 39 1 7.42 72.70 b)
Treatments compared C L (49.02)
Sabatieria punctata 91 273 26.50 26.50 Paramonohystera sp. 86 175 14.85 41.35 Sabatieria sp. A 134 74 10.86 52.21 Anoplostoma blanchardi 20 55 5.10 57.32 Innocuonema sp. 27 51 5.10 62.41 Microlaimus sp. 1 30 32 4.13 66.54 Paracanthonchus caecus 8 30 3.43 69.97
Treatments compared C H (45.61)
Table 4. Continued
Mean abundance % Cumulative
(ind. / sample) (%)
Anoplostoma blanchardi 20 52 6.61 52.48 Paracanthonchus caecus 8 27 4.76 57.24 Microlaimus sp. 1 30 38 4.25 61.49 Daptonema tenuispiculum 21 26 4.00 65.49 Theristus(D.) procerus 23 20 2.84 68.34 Parachromadorita sp. 14 5 2.61 70.94
Treatments compared L H (44.41)
Sabatieria punctata 273 161 18.45 18.45 Paramonohystera sp. 175 53 17.74 36.19 Sabatieria sp. A 74 38 6.43 42.62 Innocuonema sp. 51 28 5.46 48.08 Microlaimus sp. 1 32 38 5.21 53.30 Anoplostoma blanchardi 55 52 5.19 58.49 Paracanthonchus caecus 30 27 3.49 61.98 Theristus(D.) procerus 26 20 3.48 65.46 Daptonema tenuispiculum 16 26 3.25 68.71 Ptycholaimellus ponticus 26 9 2.67 71.37 c)
Treatments compared C L (42.20)
Paramonohystera sp. 13 105 19.25 19.25 Sabatieria punctata 124 180 16.28 35.53 Anoplostoma blanchardi 47 71 9.27 44.80 Theristus(D.) procerus 44 57 7.51 52.31 Sabatieria sp. A 35 36 4.94 57.25 Ptycholaimellus ponticus 12 28 4.18 61.43 Innocuonema sp. 35 47 4.13 65.56 Daptonema tenuispiculum 14 24 4.03 65.59
Treatments compared C H (44.29)
Paramonohystera sp. 13 83 16.67 16.67 Sabatieria punctata 124 113 15.90 32.57 Theristus(D.) procerus 44 25 8.01 40.57 Anoplostoma blanchardi 47 39 7.34 47.91 Microlaimus sp. 1 33 47 6.35 54.27 Parachromadorita sp. 3 30 5.42 59.68 Sabatieria sp. A 35 26 5.37 65.06 Innocuonema sp. 35 51 4.44 69.50
Treatments compared L H (42.09)
Fig. 5. Multidimensional scaling (MDS) ordinations (untransformed data) of nematode depth-segregated assemblages at the three experimental treatments. S5surface (0–1 cm); M5subsurface (1–5 cm); D5deep (5–10 cm).
3.4. Influence on the feeding structure of nematode assemblages
In the 0–1 cm layer of treatment H, few individuals survived and a very large variability of the relative abundance of their respective feeding groups (Fig. 6) discouraged statistical comparison between treatments. Nevertheless, a general trend of differential survival was noticeable in this sediment layer. Results suggest that microvores survived better and that epigrowth feeders were more affected (Fig. 6).
In the 5–10 cm layer, where no abundance significant differences were found between
Table 5
ANOSIM results indicating statistic value (R) and significance level ( p) of tests for differences in nematode assemblage structure between the three sediment layers (S50–1 cm; M51–5 cm; D55–10 cm) of controls and low and high density treatments at different levels of data transformation
Data transformation
None œ œœ
R p R p R p
Controls
S M 0.91 ** 0.96 ** 0.87 **
D 0.99 ** 0.93 ** 0.72 **
M D 0.46 * 0.28 * 0.12 0.20
Low
S M 1.00 ** 0.97 ** 0.76 **
D 0.94 ** 0.94 ** 0.89 **
M D 0.17 0.16 0.24 * 0.17 0.12
High
S M 1.00 ** 0.99 ** 0.95 **
D 1.00 ** 0.99 ** 0.97 **
M D 0.25 0.06 0.20 0.10 0.13 0.18
* p,0.05 ( )
Table 6
Results from SIMPER analysis of untransformed data of nematode abundances indicating the contribution (%) of each species to the mean Bray–Curtis dissimilarity term (between parenthesis) for the controls (a), and the treatments L (b) and H (c); a cut-off of 70% was employed (i.e. when 70% of the total Bray–Curtis dissimilarity term between sediment layers has been explained by the species which are listed in order of decreasing contribution).
Mean abundance % Cumulative
(ind. / sample) (%)
a)
Sediment layers compared 0–1 1–5 (63.36)
Sabatieria sp. A 2 134 20.43 20.43 Paramonohystera sp. 10 86 11.78 32.21 Eleutherolaimus sp. 76 8 11.37 43.58 Sabatieria punctata 37 91 9.57 53.15 Anoplostoma blanchardi 58 20 6.15 59.30 Paracanthonchus caecus 41 8 5.60 64.91 Desmolaimus sp. 27 3 4.03 68.94 Axonolaimus sp. 18 2 2.82 71.76
Sediment layers compared 0–1 5–10 (55.70)
Sabatieria punctata 37 124 18.17 18.17 Eleutherolaimus sp. 76 0 15.57 33.74 Sabatieria sp. A 2 35 7.28 41.02 Paracanthonchus caecus 41 6 7.23 48.25 Anoplostoma blanchardi 58 45 6.95 55.20 Theristus(D.) procerus 24 45 6.21 61.40 Desmolaimus sp. 27 6 4.67 66.08 Innocuonema sp. 27 35 3.66 69.73
Sediment layers compared 1–5 5–10 (45.67)
Sabatieria sp. A 134 35 22.06 22.06 Paramonohystera sp. 86 13 15.89 37.95 Sabatieria punctata 91 124 12.11 50.06 Theristus(D.) procerus 23 44 6.87 56.92 Anoplostoma blanchardi 20 47 6.06 62.98 Daptonema tenuispiculum 21 14 3.65 66.62 Halalaimus sp. 1 6 18 3.11 69.73 b)
Sediment layers compared 0–1 1–5 (65.72)
Sabatieria punctata 43 273 25.72 25.72 Paramonohystera sp. 4 175 18.09 43.81 Sabatieria sp. A 8 74 7.44 51.25 Eleutherolaimus sp. 69 8 6.81 58.06 Innocuonema sp. 38 51 4.61 62.68 Theristus(D.) procerus 39 26 3.99 66.67 Desmolaimus sp. 40 6 3.88 70.55
Table 6. Continued
Mean abundance % Cumulative
(ind. / sample) (%)
Sediment layers compared 0–1 5–10 (59.56)
Sabatieria punctata 43 180 19.54 19.54 Paramonohystera sp. 4 105 14.83 34.38 Eleutherolaimus sp. 69 0 10.53 44.91 Theristus(D.) procerus 39 57 7.19 52.09 Desmolaimus sp. 40 10 4.75 56.84 Innocuonema sp. 38 47 4.75 61.59 Sabatieria sp. A 8 36 4.36 65.95 Ptycholaimellus ponticus 5 28 3.63 69.58
Sediment layers compared 1–5 5–10 (40.11)
Sabatieria punctata 273 180 20.16 20.16 Paramonohystera sp. 175 105 16.74 36.90 Sabatieria sp. A 74 36 6.64 43.54 Theristus(D.) procerus 26 57 5.41 48.95 Innocuonema sp. 51 47 5.34 54.29 Microlaimus sp. 1 32 18 4.86 59.15 Anoplostoma blanchardi 55 71 4.37 63.52 Paracanthonchus caecus 30 15 3.68 67.20 Microlaimus sp. 2 17 0 2.86 70.06 c)
Sediment layers compared 0–1 1–5 (92.70)
Sabatieria punctata 3 161 28.72 28.72 Paramonohystera sp. 0 53 9.45 38.17 Anoplostoma blanchardi 3 52 7.92 46.09 Sabatieria sp. A 0 38 6.59 52.68 Microlaimus sp. 1 2 38 6.25 58.93 Innocuonema sp. 0 28 5.56 64.48 Daptonema tenuispiculum 0 26 5.47 69.95
Sediment layers compared 0–1 5–10 (92.90)
Sabatieria punctata 3 113 20.50 20.50 Paramonohystera sp. 0 83 17.39 37.88 Innocuonema sp. 0 51 11.68 49.56 Microlaimus sp. 1 2 47 7.79 57.36 Anoplostoma blanchardi 3 39 6.32 63.67 Theristus(D.) procerus 1 25 5.94 69.61
Sediment layers compared 1–5 5–10 (44.54)
Fig. 6. Mean relative abundance (mean695% CI) of nematode feeding groups (Moens and Vincx, 1997) in the different sediment layers and the whole cores; M5microvores, CF5ciliate-feeders, DF5deposit-feeders, EF5epigrowth-feeders, FP5facultative predators, P5predators.
4. Discussion
diversities of these samples were studied for the three sediment layers and compared to those of the controls collected at the end of the experiment. No statistically significant difference in these univariate measures was found between the beginning and the end of the experiment (t-test, p,0.05). Multivariate analysis (MDS) did not reveal significant differences as well.
A short term experiment offered three main advantages compared to a long term one. First of all, the data outputs reflected the effects of Nereis excluding recruitment responses of meiofauna to predation-disturbance impact. Secondly, it prevented Nereis cannibalism that might have occurred if high densities were held for relatively long periods (Clark, 1959; Reish and Alosi, 1968; Caron, 1995). Finally, it allowed the distinction of predation from sediment perturbation effects of Nereis on meiofauna.
We are aware that, although our experiment was successful in detecting Nereis effects on meiofauna, a pseudoreplication problem could have occurred due to the experimental design. More specifically, microcosm tubes essentially isolated the sediment in each replicate treatment and control. However, water above the sediment surface was able to flow between the different treatment and control replicates through the tubes’ holes covered with a 0.5-mm mesh gauze and the 2-mm mesh grids at the top of the tubes. Mobile fauna as nauplii and copepods could have been able to move between treatments and controls through these holes and grids. Although results suggest that mobile fauna migration was negligible, future experiments should be conducted by isolating the fauna of each replicate thus avoiding possible migrations between different microcosm tubes. Moreover, future experiments should be conducted with replicates (or basins) with separate water supply in order to avoid severe treatment effects, e.g., extreme mortality of Nereis in the high density treatment. The resulting decay and decomposition effects of the latter would have affected all of the treatments and the controls leading to incorrect experimental interpretations.
The large number of dead nematodes found in the surface sediment layer in treatment H suggested that Nereis sediment disturbance was a more influential process on nematode assemblages than predation. Disturbance effect on nematode abundance was greater than the estimated predation by approximately a 6:4 ratio. It can be objected, however, that predation effect may have been overestimated according to the faster decomposition that some nematode species may undergo compared to other species, even in the short time period of the experiment. In other words, the rapid decomposition rates of some species could explain the lower number of total nematodes (dead1live) in treatment H compared to controls and treatment L. As a result, a significant number of individuals of these species may have not been counted even as dead nematodes. In order to answer to this question, dead nematodes in treatment H were identified at species level and integrated with live nematodes in a MDS analysis (2d and 3d) carried out for the 0–1 cm layer and with different degrees of data transformation. The resulting plots (not reported herein for space constraints) did not show any clustering between samples of same treatments. If H samples had clustered separately from C and L samples, the time-differing decomposition hypothesis would have been supported, but this was not observed.
on meiofauna, though predation may not be selective. Olivier et al. (1993) reported that from 75 to 98% (depending on the year period) of Nereis gut content is inorganic matter. Goerke (1971) reported similar amounts (42 to 95%) of inorganic matter in Nereis gut. Swallowing large amounts of sediment in the sweep-and-plough food-searching strategy indicates that Nereis do not specifically prey on meiofauna. Predation on meiofauna is thus a consequence of swallowing sediment in an almost nonselective way.
Copepods and nauplii were both significantly affected by high densities of Nereis suggesting that Nereis impacts at least two levels of the copepod life cycle (i.e. adults and juveniles). This must be an important force acting on population dynamics in the field and requires further studies to determine its significance.
It is possible that the observed high mortality was an experimental artifact induced by the high experimental densities of Nereis. It seems unlikely that meiofauna could tolerate this high mortality in natural systems, and this question should be investigated in a field experiment. It is worth noting, however, that passive transport of meiofauna in the field may mask eventual high mortalities caused by Nereis disturbance. Several studies have shown that in soft bottoms passive transport is the primary dispersal mean of meiofauna and small sessile macrofauna, thus allowing recolonization of small disturbance patches (Fegley, 1989; Palmer, 1988; DePatra and Levin, 1989; Commito, 1995a,b). Passive dispersal in the field may then be an important process in maintaining relatively high meiofaunal abundances in high-density Nereis patches.
lower survival. This was probably due to greater availability (i.e. lower rarefaction) of microvore nematodes food items (bacteria) compared to those of epigrowth-feeding nematodes. In the 5–10 cm sediment layer, the relative abundance of microvores and deposit feeders respectively tended to increase and decrease from controls to treatment H. In this case, the cause may be the oxygenation of the deeper sediment layer resulting from the bioirrigating effect of the pumping movements of Nereis in its burrows (Goerke, 1971). Through bioirrigation, microbial growth was probably stimulated (Aller and Yingst, 1978; Eckman et al., 1981; Reichardt, 1989; Nehring et al., 1990; Grossmann and Reichardt, 1991) thus providing an increase in food allowing a proportionally greater number of microvores to survive in the deep sediment layer of treatments L and H.
The bioirrigating effect may also explain why vertical zonation of nematode species in subsurface and deep sediment layers was less evident in treatments L and H than in controls (Fig. 5). Vertical redox gradients were probably steeper in C cores causing a more marked vertical zonation of nematode species. Although vertical redox profiles were not measured, it was noted at the time of sampling that below 1 cm the sediment was slightly darker, especially in treatment C, and away from Nereis burrows in treatments L and H. Oxygenation of deeper sediment layers may also explain the greater abundance that nematodes tended to have below 1 cm depth in treatments L and H as compared to controls (Fig. 2). Although nematode recruitment processes are excluded due to the short experiment period, greatest densities in deeper sediment layers may have been a consequence of the promotive effects of Nereis burrows (Reise, 1981, 1985). The most likely of these, the more favourable redox conditions, allowed oxiphilic species to inhabit deeper sediment layers (Reise and Ax, 1979).
Our results clearly indicate that Nereis has an effect on univariate as well as on multivariate levels of nematode assemblages analyses. However, univariate measures were less sensitive than multivariate measures to the presence and density of Nereis. A greater sensitivity of multivariate measures in biological disturbance studies has been reported by other authors (Austen, 1989; Austen and Warwick, 1989; Warwick et al., 1990, 1997; Austen and Widdicombe, 1998). Univariate measures showed a significant difference among treatments only in the surface sediment layer and did not show any significant difference in deeper sediment layers. Assuming random predation of Nereis on meiofauna, which is what our results suggest, differences in diversity were mainly due to sediment disturbance associated with Nereis feeding activity. As for evenness (J9), it normally has lower values when disturbance occurs (Huston, 1979). However, in our experiment, in the 0–1 cm layer, in treatment H, J9was significantly greater than in treatment L and tended to be greater, although not statistically significantly, than in controls. This may be due to the short time period of the experiment. Surviving species in the 0–1 cm layer of treatment H did not have sufficient time to respond with recruitment processes. A longer term experiment would have probably allowed dominance to be established by the most resilient species. Multivariate measures showed that nematode assemblages were affected by the presence of Nereis not only when considering specific sediment layers, but also when considering the whole core. MDS plots showed that the presence of Nereis and its density had an influence on the dominant and intermediate abundance species.
feeding habits to those of N. virens (Goerke, 1971, 1976; Olivier, 1994), did not affect either meiofaunal univariate structure or their multivariate structure. The contrasting conclusions of Kennedy’s study and the present one can probably be explained by considering that (1) Kennedy’s experiment lasted about 6 days, which may have not been enough time to produce detectable variations of meiofaunal assemblages, and (2), Kennedy did not investigate meiofaunal abundance in the top cm of the sediment which was the most perturbed by Nereis in the present study.
In conclusion, our study showed that the polychaete N. virens affects meiofauna by sediment disturbance and predation at the sediment surface. In deeper sediment layers, however, it may be responsible for a promotive effect as a consequence of bioirrigation caused by its burrowing activity.
Acknowledgements
This study was supported by research grants from FIR (Fond Institutionnel pour la
´ ´ `
Recherche, Universite du Quebec a Rimouski) and CRSNG (Conseil de Recherche en ´
Science et Genie du Canada). We are grateful to Melanie Austen, Plymouth Marine Laboratory, for her kind assistance with the PRIMER statistical analyses. [RW]
References
Aller, R.C., Yingst, J.Y., 1978. Biochemistry of tube-dwelling: a study of the sedentary polychaete Amphitrite ornata (Leidy). J. Mar. Res. 36, 201–254.
Ambrose, Jr. W.G., 1984a. Role of predatory infauna in structuring marine soft-bottom communities. Mar. Ecol. Prog. Ser. 17, 109–115.
Ambrose, Jr. W.G., 1984b. Influence of residents on the development of a marine soft-bottom community. J. Mar. Res. 42, 633–654.
Ambrose, Jr. W.G., 1984c. Influences of predatory polychaetes and epibenthic predators on the structure of a soft-bottom community in a Maine estuary. J. Exp. Mar. Biol. Ecol. 81, 115–145.
Austen, M.C., 1989. Factors affecting estuarine meiobenthic assemblage structure: a multifactorial microcosm experiment. J. Exp. Mar. Biol. Ecol. 130, 167–187.
Austen, M.C., Widdicombe, S., 1998. Experimental evidence of effects of the heart urchin Brissopsis lyrifera on associated subtidal meiobenthic nematode communities. J. Mar. Biol. Assoc. UK 222, 219–238. Austen, M.C., Warwick, R.M., 1989. Comparison of univariate and multivariate aspects of estuarine
meiobenthic community structure. Estuar. Coast. Shelf Sci. 29, 23–42.
Branch, G.M., 1984. Competition between marine organisms: ecological and evolutionary implications. Oceanogr. Mar. Biol. Ann. Rev. 22, 429–593.
Brenchley, G.A., 1981. Disturbance and community structure: an experimental approach. J. Mar. Res. 39, 767–790.
´ ´ `
Caron, A., 1995. Etude du Partage des Ressources par Deux Annelides Polychetes, Nereis virens (Sars) et ´
Nephtys caeca (Fabricius), dans les Sediments Intertidaux de la Rive Sud de l’Estuaire Maritime du
´ ´ `
Saint-Laurent. PhD thesis, Universite du Quebec a Rimouski, p. 256. `
Caron, A., Desrosiers, G., Miron, G., Retiere, C., 1995. Comparison of spatial overlap between the polychaetes Nereis virens (Sars) and Nephtys caeca (Fabricius) in two intertidal estuarine environments. Mar. Biol. 124, 537–550.
Chareonpanich, C., Montani, S., Tsutsumi, H., Nakamura, H., 1994a. Estimation of oxygen consumption of a deposit-feeding polychaete Capitella sp. I. Fish. Sci. 60 (3), 249–251.
loaded on the sediment, as a result of the biological activity of Capitella sp. I. Mar. Poll. Bull. 28 (5), 314–318.
Clark, R.B., 1959. The tubicolous habit and the fighting reactions of the polychaete Nereis pelagica. Anim. Behav. 7, 85–90.
Clarke, K.R., Warwick, R.M., 1994. Change in Marine Communities: An Approach To Statistical Analysis and Interpretation, Plymouth Marine Laboratory, Plymouth UK.
Commito, J.A., 1982. Importance of predation by infaunal polychaetes in controlling the structure of a soft-bottom community in Maine. USA Mar. Biol. 68, 77–81.
Commito, J.A., 1995a. Dispersal dynamics in a wind-driven benthic system. Limnol. Oceanogr. 40 (8), 1513–1518.
Commito, J.A., 1995b. Dispersal dynamics of the bivalve Gemma gemma in a patchy environment. Ecol. Monogr. 65 (1), 1–20.
Commito, J.A., Shrader, P.B., 1985. Benthic community response to experimental additions of the polychaete Nereis virens. Mar. Biol. 86, 101–107.
Cullen, D.J., 1973. Bioturbation of superficial marine sediment by interstitial meiobenthos. Nature 242, 323–324.
DePatra, K.D., Levin, L.A., 1989. Evidence of the passive deposition of meiofauna into fiddler crab burrows. J. Exp. Mar. Biol. Ecol. 125, 173–192.
´
ˆ ´ `
Desrosiers, G., Brethes, J.-C., 1984. Etude de la communaute a Macoma balthica de la batture de Rimouski. Sci. Techniques l’Eau 17 (1), 25–30.
´ ˆ
Desrosiers, G., Brethes, J.-C., Culombe, F., Jacques, A., 1980. Etude Bionomique de L’endofaune Benthique
´ ´ ´
de Substrat Meuble De St.-Fabien-sur-Mer (Quebec). In: Cah. D’information, Vol. 6, Universite du Quebec
` ´ ´
a Rimouski, Departement d’Oceanographie, p. 42.
Eckman, J.E., Nowell, A.R.M., Jumars, P.A., 1981. Sediment destabilization by animal tubes. J. Mar. Res. 39, 361–374.
Fauchald, K., Jumars, P.A., 1979. The diet of worms: a study of polychaete feeding guilds. Oceanogr. Mar. Biol. Ann. Rev. 17, 193–284.
Fegley, S.R., 1989. A comparison of meiofaunal settlement onto the sediment surface and recolonization of defaunated sandy sediment. J. Exp. Mar. Biol. Ecol. 123, 97–113.
¨ ¨ ¨
Goerke, H., 1971. Die Ernahrungsweise der Nereis-Arten (Polychaeta, Nereidae) der deutschen Kusten. Veroff. Inst. Meeresforsch. Bremerh. 13, 1–50.
Goerke, H., 1976. Nereis virens (Nereidae) Nahrungsaufnahme Mit 4. Abbidungen. In: Wolf, G. (Ed.),
¨ ¨
Encyclopedia Cinematographica, Institut fur der Wissenschattlichen Film, Gottingen.
Grossmann, S., Reichardt, W., 1991. Impact of Arenicola marina on marine bacteria in intertidal sediments. Mar. Ecol. Prog. Ser. 77, 85–94.
Heip, C., Vincx, M., Vranken, G., 1985. The ecology of marine nematodes. Oceanogr. Mar. Biol. Ann. Rev. 23, 399–489.
Hopper, B.E., 1969. Marine nematodes of Canada. II. Marine nematodes from the Minas Basin–Scots Bay area of the Bay of Fundy, Nova Scotia. Can. J. Zool. 47, 671–690.
Huston, M., 1979. A general hypothesis of species diversity. Am. Nat. 113 (1), 81–101.
Kennedy, A.D., 1993. Minimal predation upon meiofauna by endobenthic macrofauna in the Exe Estuary, south west England. Mar. Biol. 117, 311–319.
Margalef, R., 1958. Information theory in ecology. Gen. Syst. 3, 36–71.
` ´
Miron, G., Desrosiers, G., Retiere, C., 1992a. Activite de prospection de son aire d’alimentation par le
` ´ ´
polychete Nereis virens (Sars) en conditions constantes d’eclairement et d’obscurite. C.R. Acad. Sci. Paris 314 (3), 455–460.
`
Miron, G., Desrosiers, G., Retiere, C., Masson, S., 1992b. Variations in time budget of the polychaete Nereis virens as a function of density and acclimatation after introduction to a new burrow. Mar. Biol. 114, 41–48. Moens, T., Vincx, M., 1997. Observations on the feeding ecology of estuarine nematodes. J. Mar. Biol. Assoc.
UK 77, 211–227.
Nehring, S., Jensen, P., Lorenzen, S., 1990. Tube-dwelling nematodes: tube construction and possible ecological effects on sediment–water interfaces. Mar. Ecol. Prog. Ser. 64, 123–128.
´ ´ ` ´ `
Olivier, M., 1994. Ethologie Comparee de l’Alimentation de Deux Especes Vicariantes de la Communaute a Macoma balthica: Nereis diversicolor (Baie du Mont Sant-Michel, France) et Nereis virens (Estuaire
´ ´ `
` ˆ
Olivier, M., Desrosiers, G., Retiere, C., Brethes, J.-C., 1993. Variations spatio–temporelles de l’alimentation du
` ´
polychete Nereis virens en zone intertidale (Estuaire maritime du saint-Laurent, Quebec). Vie Milieu 43 (1), 1–12.
Palmer, M.A., 1988. Dispersal of marine meiofauna: a review and conceptual model explaining transport and active emergence with implications for recruitment. Mar. Ecol. Prog. Ser. 48, 81–91.
Pianka, E.R., 1978. In: Evolutionary Ecology, second ed., Harper and Row, New York, p. 397.
Pielou, E.C., 1966. The measurements of diversity in different types of biological collections. J. Theor. Biol. 13, 131–144.
Platt, H.M., Warwick, R.M., 1980. The significance of free-living nematodes to the littoral ecosystem. In: Price, J.H., Irvine, D.E.G., Farnham, W.F. (Eds.), The Shore Environment, Ecosystems, Vol. 2, Academic Press, New York, pp. 729–759.
Platt, H.M., Warwick, R.M., 1983. Freeliving marine nematodes. Pt 1. British enoplids. In: Pictorial Key To World Genera and Notes For the Identification of British Species, Synopses of the British Fauna, Vol. No. 28, Cambridge University Press, Cambridge, UK.
Platt, H.M., Warwick, R.M., 1988. Freeliving marine nematodes. Pt 2. British chromadorids. In: Pictorial Key To World Genera and Notes For the Identification of British Species, Synopses of the British Fauna, Vol. No. 38, Cambridge University Press, Cambridge, UK.
Raffaelli, D., Conacher, H., McLachlan, H., Emes, C., 1989. The role of epibenthic crustacean predators in an estuarine food web. Estuar. Coast. Shelf Sci. 28, 149–160.
Reichardt, W., 1989. Microbiological aspects of bioturbation. Sci. Mar. 53, 301–306.
Reise, K., 1979. Moderate predation on meiofauna by the macrobenthos of the Wadden Sea. Helgol. Wissensch. Meeresunters. 32, 453–465.
Reise, K., 1981. High abundance of small zoobenthos around biogenic structures in tidal sediments of the Wadden Sea. Helgol. Wissensch. Meeresunters. 34, 413–425.
Reise, K., 1985. Tidal Flat Ecology, an Experimental Approach To Species Interactions. In: Ecological Studies, Vol. 54, Springer-Verlag, Berlin, p. 191.
Reise, K., Ax, P., 1979. A meiofaunal ‘‘thiobios’’ limited to the anaerobic sulfide system of marine sand does not exist. Mar. Biol. 54, 225–237.
Reish, D.J., Alosi, M.C., 1968. Aggressive behaviour in the polychaetous annelid family Nereidae. Bull. Soc. Calif. Acad. Sci. 67 (1), 21–28.
Riemann, F., Schrage, M., 1978. The mucus-trap hypothesis on feeding of aquatic nematodes and implications for biodegradation and sediment texture. Oecologia 34, 75–88.
Ronn, C., Bonsdorff, E., Nelson, W., 1988. Predation as a mechanism of interference within infauna in shallow ¨
brackish water soft bottoms, experiments with an infaunal predator Nereis diversicolor O.F. Muller. J. Exp. Mar. Biol. Ecol. 116, 143–157.
Schratzberger, M., Warwick, R.M., 1998. Effects of physical disturbance on nematode communities in sand and mud: a microcosm experiment. Mar. Biol. 150, 643–650.
Tenore, K.R., 1983. Organic nitrogen and caloric content of detritus. III Effect on growth of a deposit-feeding polychaete, Capitella capitata. Estuar. Coast. Shelf Sci. 17, 733–742.
Tsuchiya, M., Kurihara, Y., 1980. Effect of the feeding behaviour of macrobenthos on changes in environmental conditions of intertidal flats. J. Exp. Mar. Biol. Ecol. 44, 85–94.
Warwick, R.M., Platt, H.M., Clarke, K.R., Agardh, J., Gobin, J., 1990. Analysis of macrobenthic and meiobenthic community structure in relation to pollution and disturbance in Hamilton Harbour, Bermuda. J. Exp. Mar. Biol. Ecol. 138, 119–142.
Warwick, R.M., Clarke, K.R., Gee, J.M., 1997. The effect of disturbance by soldier crabs Mictyris platycheles H. Milne Edwards on meiobenthic community structure. J. Exp. Mar. Biol. Ecol. 135, 19–33.
Wilkinson, L., 1997. SYSTAT .7.0: The system for statistics, SPSS, Chicago, USA.
Wilson, Jr. W.H., 1981. Sediment-mediated interactions in a densely populated infaunal assemblage: the effects of the polychaete Abarenicola pacifica. J. Mar. Res. 39, 735–748.
